The Role of Membrane Lipids in the Formation and Function of Caveolae

Overview

Journal Cold Spring Harb Perspect Biol

Specialties Biology
Molecular Biology

Date 2023 Jun 5

PMID 37277189

Authors

Anne K Kenworthy

Bing Han

Nicholas Ariotti

Robert G Parton

Affiliations

Soon will be listed here.

Abstract

Caveolae are plasma membrane invaginations with a distinct lipid composition. Membrane lipids cooperate with the structural components of caveolae to generate a metastable surface domain. Recent studies have provided insights into the structure of essential caveolar components and how lipids are crucial for the formation, dynamics, and disassembly of caveolae. They also suggest new models for how caveolins, major structural components of caveolae, insert into membranes and interact with lipids.

Citing Articles

Lipid organization by the Caveolin-1 complex.

Liebl K, Voth G Biophys J. 2024; 123(21):3688-3697.

PMID: 39306671 PMC: 11560304. DOI: 10.1016/j.bpj.2024.09.018.

Caveolin assemblies displace one bilayer leaflet to organize and bend membranes.

Doktorova M, Daum S, Ebenhan J, Neudorf S, Han B, Sharma S bioRxiv. 2024; .

PMID: 39257813 PMC: 11383982. DOI: 10.1101/2024.08.28.610209.

Lipid Organization by the Caveolin-1 Complex.

Liebl K, Voth G bioRxiv. 2024; .

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Scaffolds and the scaffolding domain: an alternative paradigm for caveolin-1 signaling.

Lim J, Bernatchez P, Nabi I Biochem Soc Trans. 2024; 52(2):947-959.

PMID: 38526159 PMC: 11088920. DOI: 10.1042/BST20231570.

Editorial: The role of pericytes in physiology and pathophysiology.

Sandow S, Wilson S, Leo M Front Physiol. 2023; 14:1306031.

PMID: 37929215 PMC: 10625401. DOI: 10.3389/fphys.2023.1306031.

References

Yang G, Xu H, Li Z, Li F . Interactions of caveolin-1 scaffolding and intramembrane regions containing a CRAC motif with cholesterol in lipid bilayers. Biochim Biophys Acta. 2014; 1838(10):2588-99. DOI: 10.1016/j.bbamem.2014.06.018. View

Walser P, Ariotti N, Howes M, Ferguson C, Webb R, Schwudke D . Constitutive formation of caveolae in a bacterium. Cell. 2012; 150(4):752-63. DOI: 10.1016/j.cell.2012.06.042. View

Parton R, Kozlov M, Ariotti N . Caveolae and lipid sorting: Shaping the cellular response to stress. J Cell Biol. 2020; 219(4). PMC: 7147102. DOI: 10.1083/jcb.201905071. View

Hubert M, Larsson E, Vegesna N, Ahnlund M, Johansson A, Moodie L . Lipid accumulation controls the balance between surface connection and scission of caveolae. Elife. 2020; 9. PMC: 7239661. DOI: 10.7554/eLife.55038. View

Parton R . Caveolae: Structure, Function, and Relationship to Disease. Annu Rev Cell Dev Biol. 2018; 34:111-136. DOI: 10.1146/annurev-cellbio-100617-062737. View

Le Lay S, Hajduch E, Lindsay M, Le Liepvre X, Thiele C, Ferre P . Cholesterol-induced caveolin targeting to lipid droplets in adipocytes: a role for caveolar endocytosis. Traffic. 2006; 7(5):549-61. DOI: 10.1111/j.1600-0854.2006.00406.x. View

Murata M, Peranen J, Schreiner R, Wieland F, Kurzchalia T, Simons K . VIP21/caveolin is a cholesterol-binding protein. Proc Natl Acad Sci U S A. 1995; 92(22):10339-43. PMC: 40792. DOI: 10.1073/pnas.92.22.10339. View

Del Pozo M, Lolo F, Echarri A . Caveolae: Mechanosensing and mechanotransduction devices linking membrane trafficking to mechanoadaptation. Curr Opin Cell Biol. 2020; 68:113-123. DOI: 10.1016/j.ceb.2020.10.008. View

Han B, Copeland C, Kawano Y, Rosenzweig E, Austin E, Shahmirzadi L . Characterization of a caveolin-1 mutation associated with both pulmonary arterial hypertension and congenital generalized lipodystrophy. Traffic. 2016; 17(12):1297-1312. PMC: 5197452. DOI: 10.1111/tra.12452. View

10.

Li Q, Zhang Q, Wang M, Zhao S, Ma J, Luo N . Eicosapentaenoic acid modifies lipid composition in caveolae and induces translocation of endothelial nitric oxide synthase. Biochimie. 2006; 89(1):169-77. DOI: 10.1016/j.biochi.2006.10.009. View

11.

Busija A, Patel H, Insel P . Caveolins and cavins in the trafficking, maturation, and degradation of caveolae: implications for cell physiology. Am J Physiol Cell Physiol. 2017; 312(4):C459-C477. PMC: 5407024. DOI: 10.1152/ajpcell.00355.2016. View

12.

Pelkmans L, Burli T, Zerial M, Helenius A . Caveolin-stabilized membrane domains as multifunctional transport and sorting devices in endocytic membrane traffic. Cell. 2004; 118(6):767-80. DOI: 10.1016/j.cell.2004.09.003. View

13.

Kovtun O, Tillu V, Jung W, Leneva N, Ariotti N, Chaudhary N . Structural insights into the organization of the cavin membrane coat complex. Dev Cell. 2014; 31(4):405-19. DOI: 10.1016/j.devcel.2014.10.002. View

14.

Parat M, Fox P . Palmitoylation of caveolin-1 in endothelial cells is post-translational but irreversible. J Biol Chem. 2001; 276(19):15776-82. DOI: 10.1074/jbc.M006722200. View

15.

Barelli H, Antonny B . Lipid unsaturation and organelle dynamics. Curr Opin Cell Biol. 2016; 41:25-32. DOI: 10.1016/j.ceb.2016.03.012. View

16.

Sargiacomo M, Sudol M, Tang Z, Lisanti M . Signal transducing molecules and glycosyl-phosphatidylinositol-linked proteins form a caveolin-rich insoluble complex in MDCK cells. J Cell Biol. 1993; 122(4):789-807. PMC: 2119592. DOI: 10.1083/jcb.122.4.789. View

17.

Pol A, Martin S, Fernandez M, Ingelmo-Torres M, Ferguson C, Enrich C . Cholesterol and fatty acids regulate dynamic caveolin trafficking through the Golgi complex and between the cell surface and lipid bodies. Mol Biol Cell. 2005; 16(4):2091-105. PMC: 1073686. DOI: 10.1091/mbc.e04-08-0737. View

18.

Tran D, Carpentier J, Sawano F, Gorden P, Orci L . Ligands internalized through coated or noncoated invaginations follow a common intracellular pathway. Proc Natl Acad Sci U S A. 1987; 84(22):7957-61. PMC: 299455. DOI: 10.1073/pnas.84.22.7957. View

19.

Lamaze C, Tardif N, Dewulf M, Vassilopoulos S, Blouin C . The caveolae dress code: structure and signaling. Curr Opin Cell Biol. 2017; 47:117-125. DOI: 10.1016/j.ceb.2017.02.014. View

20.

Bucci M, Gratton J, Rudic R, Acevedo L, Roviezzo F, Cirino G . In vivo delivery of the caveolin-1 scaffolding domain inhibits nitric oxide synthesis and reduces inflammation. Nat Med. 2000; 6(12):1362-7. DOI: 10.1038/82176. View